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What the bird’s brain tells the bird’s eye: the function of descending input to the avian retina

Published online by Cambridge University Press:  28 April 2011

MARTIN WILSON  and
SARAH H. LINDSTROM
MARTIN WILSON*
Affiliation:
Department of Neurobiology, Physiology and Behavior, College of Biological Sciences, University of California, Davis, California
SARAH H. LINDSTROM
Affiliation:
Department of Neurobiology, Physiology and Behavior, College of Biological Sciences, University of California, Davis, California
*
*Address correspondence and reprint requests to: Martin Wilson, Department of Neurobiology, Physiology and Behavior, College of Biological Sciences, University of California, Davis, California, 95616. E-mail: mcwilson@ucdavis.edu
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Abstract

As Cajal discovered in the late 19th century, the bird retina receives a substantial input from the brain. Approximately 10,000 fibers originating in a small midbrain nucleus, the isthmo-optic nucleus (ION), terminate in each retina. The input to the ION is chiefly from the optic tectum which, in the bird, is the primary recipient of retinal input. These neural elements constitute a closed loop, the centrifugal visual system (CVS), beginning and ending in the retina, that delivers positive feedback to active ganglion cells. Several features of the system are puzzling. All fibers from the ION terminate in the ventral retina and an unusual axon-bearing amacrine cell, the target cell, is the postsynaptic partner of these fibers. While the rest of the CVS is orderly and retinotopic, target cell axons project seemingly at random, mostly to distant parts of the retina. We review here the most significant features of the anatomy and physiology of the CVS with a view to understanding its function. We suggest that many of the facts about this system, including some that are otherwise difficult to explain, can be accommodated within the hypothesis that the images of shadows cast on the ground or on objects in the environment, initiate a rapid and parallel search of the sky for a possible aerial predator. If a predator is located, shadow and predator would be temporarily linked together and tracked by the CVS.

Keywords

Centrifugal visual systemEfferent fibersAmacrine cellIsthmo-optic nucleus
Type
Perception and representation
Information
Visual Neuroscience , Volume 28 , Issue 4 , July 2011 , pp. 337 - 350
Copyright
Copyright © Cambridge University Press 2011

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References

Caro, T. (2005). Antipredator Defenses in Birds and Mammals. Chicago, IL: University of Chicago Press.Google Scholar
Catsicas, S., Catsicas, M. & Clarke, P.G. (1987). Long-distance intraretinal connections in birds. Nature 326, 186–187.CrossRefGoogle ScholarPubMed
Cellerino, A., Novelli, E. & Galli-Resta, L. (2000). Retinal ganglion cells with NADPH-diaphorase activity in the chick form a regular mosaic with a strong dorsoventral asymmetry that can be modelled by a minimal spacing rule. European Journal of Neuroscience 12, 613–620.CrossRefGoogle Scholar
Chmielewski, C.E., Dorado, M.E., Quesada, A., Geniz-Galvez, J.M. & Prada, F.A. (1988). Centrifugal fibers in the chick retina. A morphological study. Anatomia Histologia Embryologia 17, 319–327.CrossRefGoogle ScholarPubMed
Clarke, P.G. & Cowan, W.M. (1976). The development of the isthmo-optic tract in the chick, with special reference to the occurrence and correction of developmental errors in the location and connections of isthmo-optic neurons. Journal of Comparative Neurology 167, 143–164.CrossRefGoogle Scholar
Clarke, P.G., Gyger, M. & Catsicas, S. (1996). A centrifugally controlled circuit in the avian retina and its possible role in visual attention switching. Visual Neuroscience 13, 1043–1048.CrossRefGoogle ScholarPubMed
Cowan, W.M. (1970). centrifugal fibres of the avian retina. British Medical Bulletin 26, 112–118.CrossRefGoogle Scholar
Cowan, W.M. & Clarke, P.G. (1976). The development of the isthmo-optic nucleus. Brain, Behavor and Evolution 13, 345–375.CrossRefGoogle ScholarPubMed
Cowan, W.M. & Powell, T.P. (1963). Centrifugal fibres in the avian visual system. Proceedings of Royal Society London B: Biological Sciences 158, 232–252.Google ScholarPubMed
Cox, S.A., Peoples, A.D., DeMaso, S.J., Lusk, J.J. & Guthery, F.S. (2004). Survival and cause-specific mortality of northern Bobwhites in western Oklahoma. The Journal of Wildlife Management 69, 663–671.CrossRefGoogle Scholar
Cresswell, W., Butler, S., Whittingham, M.J. & Quinn, J.L. (2009). Very short delays prior to escape from potential predators may function efficiently as adaptive risk-assessment periods. Behaviour 146, 795–813.Google Scholar
Crossland, W.J., Cowan, W.M., Rogers, L.A. & Kelly, J.P. (1974). The specification of the retino-tectal projection in the chick. Journal of Comparative Neurology 155, 127–164.CrossRefGoogle ScholarPubMed
Crossland, W.J. & Hughes, C.P. (1978). Observations on the afferent and efferent connections of the avian isthmo-optic nucleus. Brain Research 145, 239–256.CrossRefGoogle ScholarPubMed
Dogiel, A.S. (1895). Die Retina der Vogel. Archiv für Mikroskopische Anatomie 44, 622–648.CrossRefGoogle Scholar
Dowling, J.E. & Cowan, W.M. (1966). An electron microscope study of normal and degenerating centrifugal fiber terminals in the pigeon retina. Zeitschrift Fuer Zellforschung Und Mikroskopische Anatomie 71, 14–28.CrossRefGoogle ScholarPubMed
Evans, C.S., Macedonia, J.M. & Marler, P. (1993). Effects of apparent size and speed on the response of chickens (Gallus gallus) to computer-generated simulations of aerial predators. Animal Behaviour 46, 1–11.CrossRefGoogle Scholar
Feyerabend, B., Malz, C.R. & Meyer, D.L. (1994). Birds that feed-on-the-wing have few isthmo-optic neurons. Neuroscience Letters 182, 66–68.CrossRefGoogle ScholarPubMed
Fischer, A.J. & Stell, W.K. (1999). Nitric oxide synthase-containing cells in the retina, pigmented epithelium, choroid, and sclera of the chick eye. Journal of Comparative Neurology 405, 1–14.3.0.CO;2-U>CrossRefGoogle ScholarPubMed
Fritzsch, B., Crapon de Caprona, M.D. & Clarke, P.G. (1990). Development of two morphological types of retinopetal fibers in chick embryos, as shown by the diffusion along axons of a carbocyanine dye in the fixed retina. Journal of Comparative Neurology 300, 405–421.CrossRefGoogle ScholarPubMed
Galifret, Y., Condé-Courtine, F., Repérant, J. & Serviere, J. (1971). Centrifugal control in the visual system of the pigeon. Vision Research, (Suppl.) 3, 185–200.CrossRefGoogle ScholarPubMed
Gastinger, M.J., Tian, N., Horvath, T. & Marshak, D.W. (2006). Retinopetal axons in mammals: Emphasis on histamine and serotonin. Current Eye Research 31, 655–667.CrossRefGoogle Scholar
Goodale, M.A. (1983). Visually guided pecking in the pigeon (Columba livia). Brain, Behavor and Evolution 22, 22–41.CrossRefGoogle ScholarPubMed
Goureau, O., Regnier-Ricard, F., Jonet, L., Jeanny, J.C., Courtois, Y. & Chany-Fournier, F. (1997). Developmental expression of nitric oxide synthase isoform I and III in chick retina. Journal of Neuroscience Research 50, 104–113.3.0.CO;2-B>CrossRefGoogle ScholarPubMed
Hackett, S.J., Kimball, R.T., Reddy, S., Bowie, R.C., Braun, E.L., Braun, M.J., Chojnowski, J.L., Cox, W.A., Han, K.L., Harshman, J., Huddleston, C.J., Marks, B.D., Miglia, K.J., Moore, W.S., Sheldon, F.H., Steadman, D.W., Witt, C.C. & Yuri, T. (2008). A phylogenomic study of birds reveals their evolutionary history. Science 320, 1763–1768.CrossRefGoogle ScholarPubMed
Hahmann, U. & Gunturkun, O. (1992). Visual-discrimination deficits after lesions of the centrifugal visual system in pigeons (Columba livia). Visual Neuroscience 9, 225–233.CrossRefGoogle ScholarPubMed
Hayes, B.P. & Holden, A.L. (1983 a). The distribution of centrifugal terminals in the pigeon retina. Experimental Brain Research 49, 189–197.Google ScholarPubMed
Hayes, B.P. & Holden, A.L. (1983 b). The distribution of displaced ganglion cells in the retina of the pigeon. Experimental Brain Research 49, 181–188.Google ScholarPubMed
Hayes, B.P. & Webster, K.E. (1981). Neurones situated outside the isthmo-optic nucleus and projecting to the eye in adult birds. Neuroscience Letters 26, 107–112.CrossRefGoogle Scholar
Hirsch, J., Lindley, R.H. & Tolman, E.C. (1955). An experimental test of an alleged innate sign stimulus. Journal of Comparative and Physiological Psychology 48, 278–280.CrossRefGoogle ScholarPubMed
Holden, A.L. (1966). Two possible visual functions for centrifugal fibres to the retina. Nature 212, 837–838.CrossRefGoogle ScholarPubMed
Holden, A.L. (1968). The centrifugal system running to the pigeon retina. Journal of Physiology 197, 199–219.CrossRefGoogle Scholar
Holden, A.L. (1970). Receptive properties of centrifugal cells projecting to the pigeon retina. Journal of Physiology 210, 155P.Google Scholar
Holden, A.L. (1990). Centrifugal pathways to the retina: Which way does the “searchlight” point? Visual Neuroscience 4, 493–495.CrossRefGoogle Scholar
Holden, A.L. & Powell, T.P. (1972). The functional organization of the isthmo-optic nucleus in the pigeon. Journal of Physiology 223, 419–447.CrossRefGoogle ScholarPubMed
Hughes, C.P. & Pearlman, A.L. (1974). Single unit receptive fields and the cellular layers of the pigeon optic tectum. Brain Research 80, 365–377.CrossRefGoogle ScholarPubMed
Knipling, R.R. (1978). No deficit in near-field visual acuity of pigeons after transection of the isthmo-optic tract. Physiology and Behavior 21, 813–816.CrossRefGoogle ScholarPubMed
Leresche, N., Hardy, O. & Jassik-Gerschenfeld, D. (1983). Receptive field properties of single cells in the pigeon’s optic tectum during cooling of the ‘visual wulst’. Brain Research 267, 225–236.CrossRefGoogle ScholarPubMed
Li, W.C., Hu, J. & Wang, S.R. (1999). Tectal afferents monosynaptically activate neurons in the pigeon isthmo-optic nucleus. Brain Research Bulletin 49, 203–208.CrossRefGoogle ScholarPubMed
Li, W. & Wang, S. (1999). Morphology and dye-coupling of cells in the pigeon isthmo-optic nucleus. Brain, Behaviour and Evolution 53, 67–74.CrossRefGoogle ScholarPubMed
Li, J.L., Xiao, Q., Fu, Y.X. & Wang, S.R. (1998). Centrifugal innervation modulates visual activity of tectal cells in pigeons. Visual Neuroscience 15, 411–415.CrossRefGoogle ScholarPubMed
Lindstrom, S.H., Azizi, N., Weller, C. & Wilson, M. (2010). Retinal input to efferent target amacrine cells in the avian retina. Visual Neuroscience 27, 103–118.CrossRefGoogle ScholarPubMed
Lindstrom, S.H., Nacsa, N., Blankenship, T., Fitzgerald, P.G., Weller, C., Vaney, D.I. & Wilson, M. (2009). Distribution and structure of efferent synapses in the chicken retina. Visual Neuroscience 26, 215–226.CrossRefGoogle ScholarPubMed
Marin, G., Letelier, J.C. & Wallman, J. (1990). Saccade-related responses of centrifugal neurons projecting to the chicken retina. Experimental Brain Research 82, 263–270.CrossRefGoogle Scholar
Martin, G.R. (1993). Producing the image. In Brain and Behaviour in Birds, ed. Zeigler, H.P. and Bischof, H-J., pp. 5–24. , Cambridge, MA: MIT Press.Google Scholar
Maturana, H.R. & Frenk, S. (1965). Synaptic connections of the centrifugal fibers in the pigeon retina. Science 150, 359–361.CrossRefGoogle ScholarPubMed
McCartney, E.S. (1947). Beneath the shadow of some bird of prey. The Classical Journal 42, 240–242.Google Scholar
McGill, J.I., Powell, T.P. & Cowan, W.M. (1966). The organization of the projection of the centrifugal fibres to the retina in the pigeon. Journal of Anatomy 100, 35–49.Google Scholar
Medina, M., Reperant, J., Miceli, D., Bertrand, C. & Bennis, M. (1998). An immunohistochemical study of putative neuromodulators and transmitters in the centrifugal visual system of the quail (Coturnix japonica). Journal of Chemical Neuroanatomy 15, 75–95.CrossRefGoogle ScholarPubMed
Miceli, D., Reperant, J., Bavikati, R., Rio, J.P. & Volle, M. (1997). Brain-stem afferents upon retinal projecting isthmo-optic and ectopic neurons of the pigeon centrifugal visual system demonstrated by retrograde transneuronal transport of rhodamine beta-isothiocyanate. Visual Neuroscience 14, 213–224.CrossRefGoogle ScholarPubMed
Miceli, D., Reperant, J., Bertrand, C. & Rio, J.P. (1999). Functional anatomy of the avian centrifugal visual system. Behavioral Brain Research 98, 203–210.CrossRefGoogle ScholarPubMed
Miceli, D., Reperant, J., Marchand, L. & Rio, J.P. (1993). Retrograde transneuronal transport of the fluorescent dye rhodamine beta-isothiocyanate from the primary and centrifugal visual systems in the pigeon. Brain Research 601, 289–298.CrossRefGoogle ScholarPubMed
Miceli, D., Reperant, J., Rio, J.P., Hains, P. & Medina, M. (2002). Serotonin immunoreactivity in the retinal projecting isthmo-optic nucleus and evidence of brainstem raphe connections in the pigeon. Brain Research 958, 122–129.CrossRefGoogle ScholarPubMed
Miceli, D., Reperant, J., Rio, J.P. & Medina, M. (1995). GABA immunoreactivity in the nucleus isthmo-opticus of the centrifugal visual system in the pigeon: A light and electron microscopic study. Visual Neuroscience 12, 425–441.CrossRefGoogle Scholar
Miles, F.A. (1972 a). Centrifugal control of the avian retina. 3. Effects of electrical stimulation of the isthmo-optic tract on the receptive field properties of retinal ganglion cells. Brain Research 48, 115–129.CrossRefGoogle ScholarPubMed
Miles, F.A. (1972 b). Centrifugal control of the avian retina. I. Receptive field properties of retinal ganglion cells. Brain Research 48, 65–92.CrossRefGoogle ScholarPubMed
Miles, F.A. (1972 c). Centrifugal control of the avian retina. II. Receptive field properties of cells in the isthmo-optic nucleus. Brain Research 48, 93–113.CrossRefGoogle ScholarPubMed
Miles, F.A. (1972 d). Centrifugal control of the avian retina. IV. Effects of reversible cold block of the isthmo-optic tract on the receptive field properties of cells in the retina and isthmo-optic nucleus. Brain Research 48, 131–145.CrossRefGoogle ScholarPubMed
Morgan, I.G., Miethke, P. & Li, Z.K. (1994). Is nitric oxide a transmitter of the centrifugal projection to the avian retina? Neuroscience Letters 168, 5–7.CrossRefGoogle Scholar
Nickla, D.L., Gottlieb, M.D., Marin, G., Rojas, X., Britto, L.R. & Wallman, J. (1994). The retinal targets of centrifugal neurons and the retinal neurons projecting to the accessory optic system. Visual Neuroscience 11, 401–409.CrossRefGoogle Scholar
Ohno, H. & Uchiyama, H. (2009). Non-visually evoked activity of isthmo-optic neurons in awake, head-unrestrained quail. Experimental Brain Research 194, 339–346.CrossRefGoogle ScholarPubMed
Palleroni, A., Hauser, M. & Marler, P. (2005). Do responses of galliform birds vary adaptively with predator size? Animal Cognition 8, 200–210.CrossRefGoogle ScholarPubMed
Pearlman, A.L. & Hughes, C.P. (1976). Functional role of efferents to the avian retina. II. Effects of reversible cooling of the isthmo-optic nucleus. Journal of Comparative Neurology 166, 123–131.CrossRefGoogle Scholar
Posada, A. & Clarke, P.G. (1999). Role of nitric oxide in a fast retrograde signal during development. Brain Research. Developmental Brain Research 114, 37–42.CrossRefGoogle Scholar
Ramón y Cajal, S. (1889). Sur la morphologie et les connexions des elements de la retine des oiseaux. Anatomischer Anzeiger 11, 111–121.Google Scholar
Ramón y Cajal, S. (1895). Sobre unos corpúsculos especiales de la retina de las aves. Actas de la Sociedad Espanola de Historia Natural 24, 128–130.Google Scholar
Ramón y Cajal, S. (1896). Nouvelles contributions à l’étude histologique de la rétine. Journal de l’Anatomie et de la Physiologie 32, 481–543.Google Scholar
Ramón y Cajal, S. (1952). Histologie du système nerveux de l’homme & des vertébrés. Madrid, Spain: Consejo Superior de Investigaciones Científicas Instituto Ramon y CajalGoogle Scholar
Ramón y Cajal, S. (1972). The Structure of the Retina. Springfield, IL: C. C. Thomas.Google Scholar
Reperant, J., Medina, M., Ward, R., Miceli, D., Kenigfest, N.B., Rio, J.P. & Vesselkin, N.P. (2007). The evolution of the centrifugal visual system of vertebrates. A cladistic analysis and new hypotheses. Brain Research Reviews 53, 161–197.CrossRefGoogle ScholarPubMed
Reperant, J., Miceli, D., Vesselkin, N.P. & Molotchnikoff, S. (1989). The centrifugal visual system of vertebrates: A century-old search reviewed. International Review of Cytology 118, 115–171.CrossRefGoogle ScholarPubMed
Reperant, J., Ward, R., Miceli, D., Rio, J.P., Medina, M., Kenigfest, N.B. & Vesselkin, N.P. (2006). The centrifugal visual system of vertebrates: A comparative analysis of its functional anatomical organization. Brain Research Reviews 52, 1–57.CrossRefGoogle ScholarPubMed
Rios, H., Lopez-Costa, J.J., Fosser, N.S., Brusco, A. & Saavedra, J.P. (2000). Development of nitric oxide neurons in the chick embryo retina. Brain Research. Developmental Brain Research 120, 17–25.CrossRefGoogle ScholarPubMed
Rogers, L.J. & Miles, F.A. (1972). Centrifugal control of the avian retina. V. Effects of lesions of the isthmo-optic nucleus on visual behaviour. Brain Research 48, 147–156.CrossRefGoogle ScholarPubMed
Shortess, G.K. & Klose, E.F. (1977). Effects of lesions involving efferent fibers to the retina in pigeons (Columba livia). Physiology and Behavior 18, 409–414.CrossRefGoogle Scholar
Sohal, G.S. & Narayanan, C.H. (1974). The development of the isthmo-optic nucleus in the duck (Anasplatyrhynchos) I. Changes in cell number and cell size during normal development. Brain Research 77, 243–255.CrossRefGoogle ScholarPubMed
Uchiyama, H. (1989). Centrifugal pathways to the retina: Influence of the optic tectum. Visual Neuroscience 3, 183–206.CrossRefGoogle Scholar
Uchiyama, H. (1999). The isthmo-optic nucleus: A possible neural substrate for visual competition. Neurocomputing 26–27, 565–571.CrossRefGoogle Scholar
Uchiyama, H., Aoki, K., Yonezawa, S., Arimura, F. & Ohno, H. (2004). Retinal target cells of the centrifugal projection from the isthmo-optic nucleus. Journal of Comparative Neurology 476, 146–153.CrossRefGoogle ScholarPubMed
Uchiyama, H. & Barlow, R.B. (1994). Centrifugal inputs enhance responses of retinal ganglion cells in the Japanese quail without changing their spatial coding properties. Vision Research 34, 2189–2194.CrossRefGoogle ScholarPubMed
Uchiyama, H. & Ito, H. (1993). Target cells for the isthmo-optic fibers in the retina of the Japanese quail. Neuroscience Letters 154, 35–38.CrossRefGoogle ScholarPubMed
Uchiyama, H., Ito, H. & Tauchi, M. (1995). Retinal neurones specific for centrifugal modulation of vision. Neuroreport 6, 889–892.CrossRefGoogle ScholarPubMed
Uchiyama, H., Matsutani, S. & Watanabe, M. (1987). Activation of the isthmo-optic neurons by the visual Wulst stimulation. Brain Research 406, 322–325.CrossRefGoogle ScholarPubMed
Uchiyama, H., Nakamura, S. & Imazono, T. (1998). Long-range competition among the neurons projecting centrifugally to the quail retina. Visual Neuroscience 15, 417–423.CrossRefGoogle Scholar
Uchiyama, H. & Stell, W.K. (2005). Association amacrine cells of Ramon y Cajal: Rediscovery and reinterpretation. Visual Neuroscience 22, 881–891.CrossRefGoogle Scholar
Uchiyama, H., Yamamoto, N. & Ito, H. (1996). Tectal neurons that participate in centrifugal control of the quail retina: A morphological study by means of retrograde labeling with biocytin. Visual Neuroscience 13, 1119–1127.CrossRefGoogle ScholarPubMed
Wallenberg, A. (1898). Das mediale Opticusbündel der Taube. Neurol Zbl 17, 532–537.Google Scholar
Weidner, C., Reperant, J., Desroches, A.M., Miceli, D. & Vesselkin, N.P. (1987). Nuclear origin of the centrifugal visual pathway in birds of prey. Brain Research 436, 153–160.CrossRefGoogle ScholarPubMed
Whittingham, M.J., Butler, S.J., Quinn, J.L. & Cresswell, W. (2004). The effect of limited visibility on vigilance behaviour and speed of predator detection: Implications for the conservation of granivorous passerines. Oikos 106, 377–385.CrossRefGoogle Scholar
Wolf-Oberhollenzer, F. (1987). A study of the centrifugal projections to the pigeon retina using two fluorescent markers. Neuroscience Letters 73, 16–20.CrossRefGoogle Scholar
Woodson, W., Reiner, A., Anderson, K. & Karten, H.J. (1991). Distribution, laminar location, and morphology of tectal neurons projecting to the isthmo-optic nucleus and the nucleus isthmi, pars parvocellularis in the pigeon (Columba livia) and chick (Gallus domesticus): A retrograde labelling study. Journal of Comparative Neurology 305, 470–488.CrossRefGoogle Scholar
Woodson, W., Shimizu, T., Wild, J.M., Schimke, J., Cox, K. & Karten, H.J. (1995). Centrifugal projections upon the retina: An anterograde tracing study in the pigeon (Columba livia). Journal of Comparative Neurology 362, 489–509.CrossRefGoogle ScholarPubMed
Wylie, D.R. & Frost, B.J. (1990). The visual response properties of neurons in the nucleus of the basal optic root of the pigeon: a quantitative analysis. Experimental Brain Research 82, 327–336.CrossRefGoogle ScholarPubMed